Skip to main content
Top
Published in: Tumor Biology 1/2014

01-01-2014 | Research Article

Prognostic significance of sphingosine kinase 2 expression in non-small cell lung cancer

Authors: Qiushi Wang, Jingyuan Li, Guanghua Li, Yinghong Li, Chunlin Xu, Ming Li, Guangquan Xu, Songbin Fu

Published in: Tumor Biology | Issue 1/2014

Login to get access

Abstract

Sphingosine kinase 2 (SphK2) as a conserved lipid kinase has not been thoroughly elucidated in non-small cell lung cancer (NSCLC). The aim of the present study was to evaluate the expression of SphK2 in NSCLC tissues and to determine its correlation with clinicopathologic characteristics and its impact on patient prognosis. We assessed the expression of SphK2 and proliferating cell nuclear antigen (PCNA) (as a proliferative index) by immunohistochemistry in 180 NSCLC patient's formalin-fixed paraffin-embedded tissue blocks. Relationship between the expression of SphK2 and PCNA and various clinicopathological features in these patients was evaluated. We detected that expression of SphK2 was gradually upregulated from normal, metaplasia/dysplasia tissues to NSCLC tissues. At the same time, PCNA expression followed a similar pattern. Statistical analysis showed that expression of SphK2 in NSCLC tissues was strongly associated with PCNA expression, histology grade, live vaccine strain invasion, lymph node status, clinical stage, tumors size, and histology type. Patients with SphK2 overexpression in their tissues had lower overall survival (OS) and disease-free survival (DFS) rates than those with low SphK2 expression. Using uni- and multivariate analysis, we found that SphK2 overexpression was an independent prognostic factor for both OS and DFS. The expression of SphK2 parallels the progression of NSCLC, and SphK2 overexpression may represent a novel and potentially independent biomarker for the prognosis of patients with NSCLC.
Literature
1.
go back to reference American Cancer Society. Cancer facts & figures 2012. Atlanta: American Cancer Society; 2012. American Cancer Society. Cancer facts & figures 2012. Atlanta: American Cancer Society; 2012.
2.
go back to reference Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, et al. The IASLC lung cancer staging project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM classification of malignant tumours. J Thorac Oncol. 2007;2:706–14.PubMedCrossRef Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, et al. The IASLC lung cancer staging project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM classification of malignant tumours. J Thorac Oncol. 2007;2:706–14.PubMedCrossRef
3.
go back to reference Ogretmen B, Hannun YA. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer. 2004;4:604–16.PubMedCrossRef Ogretmen B, Hannun YA. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer. 2004;4:604–16.PubMedCrossRef
5.
go back to reference Igarashi N, Okada T, Hayashi S, Fujita T, Jahangeer S, Nakamura SI. Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J Biol Chem. 2003;278:46832–9.PubMedCrossRef Igarashi N, Okada T, Hayashi S, Fujita T, Jahangeer S, Nakamura SI. Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J Biol Chem. 2003;278:46832–9.PubMedCrossRef
6.
go back to reference Liu H, Toman RE, Goparaju S, Maceyka M, Nava VE, Sankala H, et al. Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J Biol Chem. 2003;278:40330–6.PubMedCrossRef Liu H, Toman RE, Goparaju S, Maceyka M, Nava VE, Sankala H, et al. Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J Biol Chem. 2003;278:40330–6.PubMedCrossRef
7.
go back to reference Van Brocklyn JR, Jackson CA, Pearl DK, Kotur MS, Snyder PJ, Prior TWJ. Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme: roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J Neuropathol Exp Neurol. 2005;64:695–705.PubMedCrossRef Van Brocklyn JR, Jackson CA, Pearl DK, Kotur MS, Snyder PJ, Prior TWJ. Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme: roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J Neuropathol Exp Neurol. 2005;64:695–705.PubMedCrossRef
8.
go back to reference Sankala HM, Hait NC, Paugh SW, Shida D, Lepine S, Elmore LW, et al. Involvement of sphingosine kinase 2 in p53-independent induction of p21 by the chemotherapeutic drug doxorubicin. Cancer Res. 2007;67:10466–74.PubMedCrossRef Sankala HM, Hait NC, Paugh SW, Shida D, Lepine S, Elmore LW, et al. Involvement of sphingosine kinase 2 in p53-independent induction of p21 by the chemotherapeutic drug doxorubicin. Cancer Res. 2007;67:10466–74.PubMedCrossRef
9.
go back to reference Hait NC, Sarkar S, Le Stunff H, Mikami A, Maceyka M, Milstien S, et al. Role of sphingosine kinase 2 in cell migration toward epidermal growth factor. J Biol Chem. 2005;280:29462–9.PubMedCrossRef Hait NC, Sarkar S, Le Stunff H, Mikami A, Maceyka M, Milstien S, et al. Role of sphingosine kinase 2 in cell migration toward epidermal growth factor. J Biol Chem. 2005;280:29462–9.PubMedCrossRef
10.
go back to reference Wu J, Zhou J, Yao L, Lang Y, Liang Y, Chen L, et al. High expression of M3 muscarinic acetylcholine receptor is a novel biomarker of poor prognostic in patients with non-small cell lung cancer. Tumor Biol. 2013. doi:10.1007/s13277-013-0982-x. Wu J, Zhou J, Yao L, Lang Y, Liang Y, Chen L, et al. High expression of M3 muscarinic acetylcholine receptor is a novel biomarker of poor prognostic in patients with non-small cell lung cancer. Tumor Biol. 2013. doi:10.​1007/​s13277-013-0982-x.
11.
go back to reference Kuwabara K, Matsuda S, Fushimi K, et al. Differences in practice patterns and costs between small cell and non-small cell lung cancer patients in Japan. Tohoku J Exp Med. 2009;217:29–35.PubMedCrossRef Kuwabara K, Matsuda S, Fushimi K, et al. Differences in practice patterns and costs between small cell and non-small cell lung cancer patients in Japan. Tohoku J Exp Med. 2009;217:29–35.PubMedCrossRef
12.
go back to reference Cuvillier O, Pirianov G, Kleuser B, et al. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 1996;381:800–3.PubMedCrossRef Cuvillier O, Pirianov G, Kleuser B, et al. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 1996;381:800–3.PubMedCrossRef
13.
go back to reference Mandala SM, Thornton R, Tu Z, et al. Sphingoid base 1-phosphate phosphatase: a key regulator of sphingolipid metabolism and stress response. Proc Natl Acad Sci U S A. 1998;95:150–5.PubMedCentralPubMedCrossRef Mandala SM, Thornton R, Tu Z, et al. Sphingoid base 1-phosphate phosphatase: a key regulator of sphingolipid metabolism and stress response. Proc Natl Acad Sci U S A. 1998;95:150–5.PubMedCentralPubMedCrossRef
14.
go back to reference Olivera A, Kohama T, Edsall L, et al. Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J Cell Biol. 1999;147:545–58.PubMedCrossRef Olivera A, Kohama T, Edsall L, et al. Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J Cell Biol. 1999;147:545–58.PubMedCrossRef
15.
go back to reference Kawamori T, Kaneshiro T, Okumura M, et al. Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J. 2009;23:405–14.PubMedCrossRef Kawamori T, Kaneshiro T, Okumura M, et al. Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J. 2009;23:405–14.PubMedCrossRef
16.
go back to reference Li J, Guan HY, Gong LY, et al. Clinical significance of sphingosine kinase-1 expression in human astrocytomas progression and overall patient survival. Clin Cancer Res. 2008;14:6996–7003.PubMedCrossRef Li J, Guan HY, Gong LY, et al. Clinical significance of sphingosine kinase-1 expression in human astrocytomas progression and overall patient survival. Clin Cancer Res. 2008;14:6996–7003.PubMedCrossRef
17.
18.
go back to reference Park HW, Song JY, Kim KS, et al. Enhancement of radiosensitivity by combined ceramide and dimethylsphingosine treatment in lung cancer cells. Exp Mol Med. 2004;36:411–9.PubMedCrossRef Park HW, Song JY, Kim KS, et al. Enhancement of radiosensitivity by combined ceramide and dimethylsphingosine treatment in lung cancer cells. Exp Mol Med. 2004;36:411–9.PubMedCrossRef
19.
go back to reference Ruckhäberle E, Rody A, Engels K, Gaetje R, von Minckwitz G, Schiffmann S, et al. Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res Treat. 2007;112:41–52.PubMedCrossRef Ruckhäberle E, Rody A, Engels K, Gaetje R, von Minckwitz G, Schiffmann S, et al. Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res Treat. 2007;112:41–52.PubMedCrossRef
20.
go back to reference Facchinetti MM, Gandini NA, Fermento ME, et al. The expression of sphingosine kinase-1 in head and neck carcinoma. Cells Tissues Organs. 2010;192:314–24.PubMedCrossRef Facchinetti MM, Gandini NA, Fermento ME, et al. The expression of sphingosine kinase-1 in head and neck carcinoma. Cells Tissues Organs. 2010;192:314–24.PubMedCrossRef
21.
go back to reference Miller AV, Alvarez SE, Spiegel S, Lebman DA. Sphingosine kinases and sphingosine-1-phosphate are critical for transforming growth factor beta-induced extracellular signal-regulated kinase 1 and 2 activation and promotion of migration and invasion of esophageal cancer cells. Mol Cell Biol. 2008;28:4142–51.PubMedCentralPubMedCrossRef Miller AV, Alvarez SE, Spiegel S, Lebman DA. Sphingosine kinases and sphingosine-1-phosphate are critical for transforming growth factor beta-induced extracellular signal-regulated kinase 1 and 2 activation and promotion of migration and invasion of esophageal cancer cells. Mol Cell Biol. 2008;28:4142–51.PubMedCentralPubMedCrossRef
22.
go back to reference Cai J, Wu Y, Li C, Feng M, Shi Q, Li R, et al. Panax ginseng polysaccharide suppresses metastasis via modulating Twist expression in gastric cancer. Int J Biol Macromol. 2013;57:22–5.PubMedCrossRef Cai J, Wu Y, Li C, Feng M, Shi Q, Li R, et al. Panax ginseng polysaccharide suppresses metastasis via modulating Twist expression in gastric cancer. Int J Biol Macromol. 2013;57:22–5.PubMedCrossRef
23.
go back to reference Li C, Cai J, Geng J, Li Y, Wang Z, Li R. Purification, characterization and anticancer activity of a polysaccharide from Panax ginseng. Int J Biol Macromol. 2012;51:968–73.PubMedCrossRef Li C, Cai J, Geng J, Li Y, Wang Z, Li R. Purification, characterization and anticancer activity of a polysaccharide from Panax ginseng. Int J Biol Macromol. 2012;51:968–73.PubMedCrossRef
24.
go back to reference Wu J, Zhou J, Lang Y, Yao L, Xu H, Shi H, et al. A polysaccharide from Armillaria mellea exhibits strong in vitro anticancer activity via apoptosis-involved mechanisms. Int J Biol Macromol. 2012;51:663–7.PubMedCrossRef Wu J, Zhou J, Lang Y, Yao L, Xu H, Shi H, et al. A polysaccharide from Armillaria mellea exhibits strong in vitro anticancer activity via apoptosis-involved mechanisms. Int J Biol Macromol. 2012;51:663–7.PubMedCrossRef
25.
go back to reference Wenjing Z, Bo H, Yun S, Zhenyu W, Xiuhua Y. Immunoregulatory effects of a glucogalactan from the root of Panax quinquefolium L. Carbohydr Polym. 2012;87:2725–9.CrossRef Wenjing Z, Bo H, Yun S, Zhenyu W, Xiuhua Y. Immunoregulatory effects of a glucogalactan from the root of Panax quinquefolium L. Carbohydr Polym. 2012;87:2725–9.CrossRef
26.
go back to reference Kramer-Marek G, Capala J. The role of nuclear medicine in modern therapy of cancer. Tumor Biol. 2012;33:629–40.CrossRef Kramer-Marek G, Capala J. The role of nuclear medicine in modern therapy of cancer. Tumor Biol. 2012;33:629–40.CrossRef
27.
go back to reference French KJ, Zhuang Y, Maines LW, Gao P, Wang W, Beljanski V, et al. Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J Pharmacol Exp Ther. 2010;333:129–39.PubMedCrossRef French KJ, Zhuang Y, Maines LW, Gao P, Wang W, Beljanski V, et al. Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J Pharmacol Exp Ther. 2010;333:129–39.PubMedCrossRef
Metadata
Title
Prognostic significance of sphingosine kinase 2 expression in non-small cell lung cancer
Authors
Qiushi Wang
Jingyuan Li
Guanghua Li
Yinghong Li
Chunlin Xu
Ming Li
Guangquan Xu
Songbin Fu
Publication date
01-01-2014
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 1/2014
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-013-1051-1

Other articles of this Issue 1/2014

Tumor Biology 1/2014 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine